F OLQ J 3 D WWH UQ V ' LIIH U % H WZ H H Q ,F H ) UH H ... · Mildred Ascanio* Antarctic studies have indicated that during summer, ice-free areas experience greater Rafael Herrera*‡

Do P Cycling Patterns Differ Between Ice-Free Areas andGlacial Boundaries in the Maritime Antarctic Region?

Authors: Chacón, Noemí, Ascanio, Mildred, Herrera, Rafael, Benzo,Diana, Flores, Saúl, et al.

Source: Arctic, Antarctic, and Alpine Research, 45(2) : 190-200

Published By: Institute of Arctic and Alpine Research (INSTAAR),University of Colorado

URL: https://doi.org/10.1657/1938-4246-45.2.190

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Arctic, Antarctic, and Alpine Research, Vol. 45, No. 2, 2013, pp. 190–200

Do P Cycling Patterns Differ between Ice-Free Areas andGlacial Boundaries in the Maritime Antarctic Region?

AbstractNoemı Chacon*†§Antarctic studies have indicated that during summer, ice-free areas experience greaterMildred Ascanio*temperatures than those along the glacial boundaries. This allows for the availability of

Rafael Herrera*‡ liquid water and thus influences the biogeochemical processes of Antarctic terrestrialDiana Benzo* ecosystems. In this study we explore whether the patterns of soil phosphorus cycling differ

between the glacial boundary and ice-free areas. To do so, we chose two sites on theSaul Flores*Fildes Peninsula in Antarctica, one at the boundary of the Collins Glacier and another

Soraya J. Silva† and within an ice-free area close to Lake Uruguay. In each location, we determined soil phos-Belkis Garcıa* phorus distribution, iron and aluminum fractions, soil mineralogy, alkaline phosphatase

activity, and fluorescein diacetate hydrolysis. The results showed that soils of the ice-free*Centro de Ecologıa, Institutoarea had a greater content of phosphorus sorbed on iron/aluminum oxyhydroxides andVenezolano de Investigaciones

Cientıficas, Apdo. 20632 occluded forms. An opposite pattern was obtained for the calcium-bound phosphorusCaracas 1020-A, Venezuela pool. Accordingly, soil samples from the ice-free area showed the greatest levels of iron/†Centro de Oceanologıa y Estudios aluminum oxyhydroxides and the presence of secondary minerals such as hematite andAntarticos, Instituto Venezolano de

the intergrade chlorite-vermiculite-montmorillonite. Alkaline phosphatase activity and theInvestigaciones Cientıficas, Apdo. 20632fluorescein diacetate hydrolysis were also favored at the ice-free area. The overall resultsCaracas 1020-A, Venezuela

‡Grupo de Evaluacion y Restauracion de suggest that the less extreme microclimatic conditions and the presence of liquid waterSistemas Agrıcolas y Forestales, in the ice-free area promote the biogeochemical cycling of soil phosphorus. In a contextUniversidad de Cordoba, Edf. Leonardo of climate warming this study may contribute to the comprehension of how the expansionda Vinci s/n, Campus Universitario de

of the ice-free areas due to glacial retreat influences biogeochemical cycling of essentialRabanales, 14071 Cordoba, Spainnutrients in the Antarctic Peninsula.§Corresponding author:

[email protected]

DOI: http://dx.doi.org/10.1657/1938-4246-45.2.190

Introduction

A number of studies have concluded that Antarctic soils cansustain communities of heterotrophic organisms in spite of the ex-tremely low temperatures and dry conditions to which they areexposed (i.e., Burkins et al., 2000, 2001; Hopkins et al., 2006a,2006b; Hopkins et al., 2008). These findings have given rise toseveral research projects focused on the biotic and/or abiotic factorsdriving the soil nutrient cycling in the terrestrial ecosystems ofthis region (i.e. Tscherko et al., 2003; Barrett et al., 2005, 2006;Gajananda, 2007; Hogg et al., 2006; Hopkins et al., 2006a, 2006b;Aislabie et al., 2008; Cannone et al., 2008).

Among the essential nutrients, phosphorus (P) is consideredto be the element that most commonly limits net primary productiv-ity in various soil conditions (Vitousek, 1984; Hinsinger, 2001).This is a consequence of its poor mobility due to high reactivitywith numerous soil constituents such as iron (Fe) and aluminum(Al) oxyhydroxides, calcium (Ca), organic matter, and clay min-erals (Hinsinger, 2001; Chacon and Dezzeo, 2004). In soils of theAntarctic continent there is some controversy regarding P as alimitation. In Antarctic field experiments it has been shown thatprimary productivity increases mainly by the addition of nutrientssuch as nitrogen (N) and P (Wasley et al., 2006; Hopkins et al.,2008). However, the elevated levels of available P, and the low C:P ratio of these soils, allowed other authors to suggest that P is notbiologically limiting in the terrestrial ecosystems of this region(Bate et al., 2008). Nevertheless, it is well recognized that soils

190 / ARCTIC, ANTARCTIC, AND ALPINE RESEARCH � 2013 Regents of the University of Colorado1523-0430/6 $7.00

adjacent to Antarctic streams and lakes can be a significant sourceof available P to these biologically P limiting waters (i.e. Priscu,1995; Dore and Priscu, 2001; Barrett et al., 2009).

Soil P is generally characterized by various pools that are afunction of the state of soil development; whereas the primaryinorganic pool is characteristic of young soils, the secondary inor-ganic- and organic-P pools predominate in more mature soils(Walker and Syers, 1976). Previous studies have shown that soildevelopment is the result of the interplay among parent material,topography, climate, organisms, and time (i.e. Jenny, 1941; Kellyand Yonker, 2005; Bockheim et al., 2005). However, several au-thors agree that climate (temperature and humidity) plays an impor-tant role in soil formation because it controls the rate of physical,chemical, and biological soil processes (Cooper, 1960; Birkelandet al., 1989; Kelly and Yonker, 2005; Egli et al., 2006a; Barrett etal., 2009). In fact, in non-Antarctic cold regions the rate of soilevolution is considered to be distinctly determined by the availabil-ity and flow of soil water (Egli et al., 2003; 2006a, 2006b). How-ever, in Antarctic regions, where the liquid water availability isrestricted to austral summer (Chen and Blume, 2000; Gooseff etal., 2003), several authors have also recognized that climate is themain driving factor of soil genesis (Ugolini, 1963; Everett, 1976;Matsuoka, 1995; Zhao and Li, 1996; Chen and Blume, 1999;Gooseff et al., 2003; Cannone et al., 2008; Navas et al., 2008;Barrett et al., 2009; Bolter, 2011; Lopez-Martınez et al., 2012).

Taking into account the above findings, in Antarctic terrestrialecosystems it is expected that P distribution could be affected by


climate. In this region only two studies have reported the soil Pfractions (Blecker et al., 2006; Bate et al., 2008), and, in both,authors concluded that this element lies mainly in the primary inor-ganic pool. However, Blecker et al. (2006) indicated that differ-ences in the weathering intensity between sites account for spatialvariability in the soil P pools; while Bate et al. (2008) proposedthat geologic legacies strongly influence the soil P distribution. Itis noteworthy that these studies are restricted to continental sitesin Antarctica, while for maritime Antarctica this question remainsunclear.

Based on studies from maritime Antarctica, Ugolini and Bock-heim (2008) provided considerable evidence for climate warmingin this region. Some authors have characterized these climate condi-tions as the warmest and moistest within Antarctica (i.e. Ferron etal., 2004; Ugolini and Bockheim, 2008; Navas et al., 2008). Despitetheir sensitivity to climate warming, most areas of this region arestill covered by glaciers (Lee et al., 2004), while the ice- and snow-free areas are scarce (Navas et al., 2008). There are strong microcli-matic differences between glaciers and the ice- and snow-free areas.During the summer months, the relatively greater temperature ofthe ice- and snow-free areas leads to a deep thawing period thatproduces a more favorable supply of liquid water (Chen and Blume,2000; Gooseff et al., 2003). In contrast, in terrestrial areas adjacentto subsurface ice, liquid water is limited to the warmest hours ofthe day (Motta and Motta, 2004).

Taking into account these findings and the role of water avail-ability in the evolution of the Antarctic soils, we asked whetherthere were significant differences in the geochemical cycling ofsoil P between sites near glacial boundaries and those on ice-freeareas. Were they to exist, we hypothesized that the concentrationof several inorganic P pools defined as P sorbed on amorphousand some crystalline Al and Fe oxyhydroxides and occluded formsshould show greater values in the ice-free areas. An opposite trendis expected for the Ca-bound P pool.

In addition to the foregoing hypothesis concerning the chemi-cally defined P fractions, we also hypothesized that biological cy-cling of P should be favored in the ice-free areas. Support for thisassumption comes from the research of Barrett et al. (2006, 2009),Gajananda (2007), Zeglin et al. (2009), and Bolter (2011), whohave pointed out that due to the absence of higher plants, soilcommunities in terrestrial Antarctic ecosystems are largely con-trolled by abiotic factors. In principle, in those areas with greaterliquid water availability due to increasing temperatures, biotic ac-tivity would be enhanced. Thus, in order to test these hypotheses,we chose a site along the boundary of the Bellingshausen Ice Dome(Collins Glacier) and another in an ice-free area in the vicinity ofLake Uruguay, Antarctica.

Materials and MethodsSTUDY AREA AND SAMPLE COLLECTION

The study site was located in the vicinity of the Artigas Antarc-tic Scientific Base (Base Cientıfica Antartica Artigas [BCAA]) onthe Fildes Peninsula of King George Island, which forms part ofthe South Shetland Islands in Maritime Antarctica (61�54′–

NOEMI CHACON ET AL. / 191

62�16′S; Fig. 1). The climate is maritime with an annual meanprecipitation and temperature of 800 mm and �2 �C (1989–2001;Navas et al., 2008), respectively. During summer the temperaturesof the surface soils can reach more than 10 �C (Zhao and Li, 1996).Vegetation consists of lichens, mosses, algae, and the grass,Deschampsia antarctica (Soave et al., 2000).

The Fildes Peninsula, located at the extreme southwest of KingGeorge Island, is the largest ice-free area on the island (Soave etal., 2000; Vogt and Braun, 2004). In this region the last deglaciationoccurred at 8–5 ka B.P. (Lopez-Martınez et al., 2012). The penin-sula consists of a thick subalkaline volcanic rock stratum with inter-calations of volcaniclastic rock that characterize the Fildes Penin-sula Group (Almeida et al., 2003). According to Zhao and Li(1996), soil development at this site is controlled by the parentmaterial, landforms, and bioclimatic factors. Soils of the FildesPeninsula are composed of Histosols, Regosols, Cambisols, andAndisols (Chen and Blume, 1999).

The soil samples were collected from two sites in the vicinityof BCAA: one at the boundary of the Collins Glacier (BG:62�10′49.62�S, 58�54′34.75�W) and the other in an ice-free area(IFA: 62�11′08.33�S, 58�54′33.02�W) near Lake Uruguay (Fig. 1).We considered only one study site for the ice-free area and anotherone for the boundary of the glacier because genuine replicates ofthese sites were not feasible in widely spaced geographic areas.The lack of field replication and consequently the risk of pseudo-replication are almost inevitable in the studies of large-scale sys-tems (i.e. rivers, small watersheds, forest patches) (Hargrove andPickering, 1992; Oksanen, 2001) such as these. We think this levelof pseudo-replication in our study does not undermine our results,though it does mean they should be interpreted with caution, asother authors in similar situations have pointed out.

In each study site, we sampled the surface mineral horizon(0–10 cm) from 15 points selected according to a completely ran-dom design (total n � 30). The sampling depth was limited to 10cm due to the presence of stones and rocks. The samples werestored in plastic bags. While those samples destined for the analysisof microbial and enzymatic activity were maintained at �4 �C, thesamples for chemical analysis were air dried at room temperature(Tscherko et al., 2003). A preliminary analysis showed that soiltextural class was similar between sites; however, other soil proper-ties such as pH and organic carbon content (OC), showed differ-ences (Benzo et al., unpublished data; samples collected in 2009;Table 1). During the sampling, the field temperatures recordedat lakes adjacent to BG and IFA sites were 2.4 �C and 5.3 �C,respectively.

P FRACTIONS

Soil P fractions were obtained according to the method ofHedley et al. (1982), which was modified by Tiessen and Moir(1993). This procedure uses a sequence of increasingly strong re-agents to remove the labile and more stable P forms (Tiessen andMoir, 1993). Aliquots of 0.50 g of dry soil previously ground andsieved (0.43 mm) were sequentially extracted with anion exchangeresin, followed by 0.5 M NaHCO3, 0.1 M NaOH, 0.5 M HCl, andhot concentrated HCl. Total P was determined in aliquots of eachextract by digestion with ammonium persulphate and H2SO4 toconvert all the organic P forms (Po) to inorganic P forms (Pi).


FIGURE 1. Map of King George Island showing the relative locations of the studied sites. BCAA� Base Cientıfica Antartica Artigas,BG � boundary of the glacier, IFA � ice-free area. Digitalized image from the Letter 1111: Artigas Antarctic Scientific Base (Service ofOceanography, Hydrography and Meteorology of the Navy of Uruguay, 1991).

Another aliquot of each extract was used to measure Pi after acidifi-cation with H2SO4 to precipitate organic matter. In each extract,the pH was adjusted, and the P concentration was determined color-imetrically by means of the molybdate-ascorbic acid procedure(Murphy and Riley, 1962). Organic phosphorus was calculated asthe difference between total P and Pi. According to Tiessen andMoir (1993), soil P fractions obtained by this procedure have beenassociated with the following operationally defined pools: (i) Pextracted with resin is often considered as the labile P; (ii) bicarbon-

TABLE 1

Some soil properties in the boundary of the glacier (BG) and inthe ice-free area (IFA) (D. Benzo et al., unpublished data).

Soil properties BG IFA

pH 8.18 � 0.08a 7.18 � 0.05b

% OC 1.13 � 0.36a 0.09 � 0.03b

% Clay 6a 2b

% Silt 8a 3b

% Sand 86b 95a

Textural class Sandy Sandy

Mean values � 1 SE followed by different letters in rows denotesignificant differences between sites. OC � organic carbon.

192 / ARCTIC, ANTARCTIC, AND ALPINE RESEARCH

ate- and hydroxide-extractable P are distinguished as labile andmoderately labile P forms respectively, associated to Fe/Al oxyhy-droxides; (iii) diluted HCl P is associated with the primary mineraland/or Ca-bound P; and (iv) hot concentrated HCl P is defined asthe highly resistant and unavailable P.

Al AND Fe FRACTIONS

A sequential selective dissolution method was used to estimatethe organically bound, non-crystalline and crystalline forms of Feand Al (Wieder and Lang, 1986). Organically bound Fe and Alwere extracted with sodium pyrophosphate (FeP, AlP) (McKeague,1967). Poor crystalline forms of Fe and Al (FeO, AlO) were obtainedby extracting the soil with ammonium oxalate (pH � 4 in thedark) (McKeague and Day, 1966), and highly structured Fe and Alassociated with crystalline Fe oxides were extracted with dithionite-citrate-bicarbonate (FeDCB, AlDCB) following the method of Mehraand Jackson (1960). Concentrations of both elements in each ex-tract were determined using atomic absorption spectroscopy.

SOIL MINERALOGY

Soil mineralogy was obtained via X-ray diffraction (XRD)using Cu-K� radiation. Four representative soil samples from each


study site were made into pressed powder pellets for XRD analysis.Samples were mounted on glass plates and analyzed from 5� to90� 2� with a speed of 2� 2� per minute. The software codePDFWIN for windows was used for the evaluation of diffractionpatterns.

BIOLOGICAL AND BIOCHEMICAL ANALYSIS

In this study, the activity of alkaline phosphatase (AP) wasmeasured as an index of organic P mineralization (Dick and Tabata-bai, 1993), while the fluorescein diacetate (FD) hydrolysis wasused as a measure of soil microbial activity (Schnurer and Rosswall,1982; Green et al., 2006). In alkaline soils such as at the two studysites, it is advisable to measure the activity of AP because it isusually greater than that of the acid phosphatase (Eivazi and Tabata-bai, 1977). Briefly, aliquots of fresh soil after incubation at �37�C were used to assess FD hydrolysis and AP activity followingthe procedures of Schnurer and Rosswall (1982) and Tabatabai andBremner (1969), respectively.

STATISTICAL ANALYSIS

A one-way analysis of variance (ANOVA) was used to com-pare soil P fractions, Fe and Al forms, and microbial and biochemi-cal (fluorescein diacetate hydrolysis and alkaline phosphatase) ac-tivities. When necessary, data were log-transformed to meet theassumptions of ANOVA (NaOH-Pi, AlT, FDA). The Tukey HonestSignificant Difference (HSD) test was used as a means separationprocedure. The Mann Whitney non-parametric test was used whenthe data did not meet ANOVA assumptions (resin-Pi, NaHCO3-Pi, NaOH-Po, HClconc-Po, AlO, AlDCB, AlO/AlDCB). Pearson’s cor-relation coefficient (r) was used to examine the relationship amongparameters (soil P fractions, and microbial and biochemical activi-ties versus P pools). Univariate analyses were performed usingSTATISTICA for Windows 6.0 (Statistica, 2001).

We used a Principal Component Analysis (PCA) to determineif the concentration of soil inorganic P pools can discriminate be-tween sites influenced by glaciers and the ice-free areas. PCA wasperformed using the software Multi-Variate Statistical Package(MVSP 3.0 for Windows; Kovach, 1998).

ResultsSOIL P FRACTIONS

Concentrations of soil P in the various fractions at bothsites are summarized in Table 2. The soil from the BG had lessP in the resin-Pi fraction. No difference (P � 0.05) betweensites was observed among the mean values of NaHCO3-Pi. Noneof the sampled sites showed significant differences (P � 0.05)in organic P fractions (NaHCO3-, NaOH-, HClconc-). The concen-tration of NaOH-Pi fraction, which is associated with the Pstrongly chemisorbed on amorphous and some crystalline Al andFe phosphates (Tiessen et al., 1983), increased significantly inIFA. The soil at IFA also contained greater P in the concentratedHCl-Pi fraction.


TABLE 2

Values of soil phosphorus fractions (mg kg–1) in the boundary ofthe glacier (BG) and in the ice-free area (IFA).

Fraction BG IFA

Resin-Pi 27.48 � 1.32b 47.88 � 4.06a

NaHCO3-Pi 0.96 � 0.19a 3.00 � 1.34a

NaOH-Pi 2.96 � 0.43b 24.30 � 12.91a

HCl(dil)-Pi 385.89 � 9.21a 281.75 � 16.72b

HCl(conc)-Pi 26.80 � 1.97b 39.15 � 1.68a

NaHCO3-Po 7.95 � 1.70a 8.46 � 2.57a

NaOH-Po 1.98 � 0.41a 9.47 � 5.97a

HCl-Po 0.68 � 0.35a 2.52 � 1.03a

Mean values � 1 SE followed by different letters in rows denotesignificant differences between sites. Pi � inorganic phosphorus;Po� organic phosphorus.

One important difference between sites was that soil of theIFA, which contained greater P concentrations in NaOH-Pi andHClconc-Pi fractions, had lower P in the diluted HCl-Pi fraction,which is linked to unweathered Ca-bound P phases. At this site theweathering of primary minerals seemed to yield soluble P because apositive correlation (r � 0.63, P � 0.05; n � 15) was obtainedbetween resin-Pi and the diluted HCl-Pi fractions. Both parameterswere not correlated at the BG site (r � –0.03, P � 0.05; n �

15). Soil from the IFA also showed a negative correlation betweenNaOH-Pi and the diluted HCl-Pi fraction (r � �0.77, P � 0.05;n � 15). This correlation was not observed in the BG soil (r �

0.09, P � 0.05; n � 15).Principal Component Analyses (PCA) of the soil inorganic P

fractions from the two studied sites is shown in Figure 2. Only thefirst two axes of ordination are illustrated; these accounted for65.0% of the variance (Table 3). This analysis clearly showed that,whereas the BG site was associated with soils showing high concen-tration of the diluted HCl-Pi and low concentrations of resin-,NaHCO3-, NaOH-, and concentrated HCl-Pi fractions, the IFAfindings were opposite.

IRON AND ALUMINUM FRACTIONS

The results of the organically bound, non-crystalline and crys-talline forms of Fe and Al are presented in Table 4. In the BG site,the content of total extractable iron (FeT � FeP � FeO � FeDCB)was well above the total extractable aluminum (AlT � AlP � AlO� AlDCB); however, in the IFA they were in the same order ofmagnitude.

In both sites, the content of organically bound forms of Feand Al (FeP, AlP) was low and their contributions to the contentof FeT and AlT were as follows: BG: FeP � 1.8%, AlP � 11.7%;IFA: FeP � 3.2%, AlP � 13.5%. Comparisons of mean valuesbetween BG and IFA revealed no significant differences (P � 0.05)for FeP, whereas AlP increased sharply in the IFA soil. Poorlycrystalline forms of Fe and Al (FeO, AlO) followed a trend similarto that of the FeP and AlP fractions. The greatest content of crystal-line Fe (FeDCB) was found in the BG soil; however, there was nodifference in the content of crystalline Al (AlDCB) between sites.Non-crystallinity ratios (AlO/AlDCB, FeO/FeDCB), interpreted as the


resin-Pi

NaHCO3-Pi

NaOH-Pi

HCl-Pi

HClconc-Pi

BG

BG

BGBG

BG

BG

BG

BG

BG

BG

BG

BG

BG

BG

BG

IFA

IFA

IFA

IFA

IFA

IFA

IFA

IFA

IFA

IFA

IFA

IFA

IFA

-1,8 -1,5 -1,2 -0,9 -0,6 -0,3 0,3 0,6 0,9 1,2 1,5 1,8

Component 1

-3

-2,4

-1,8

-1,2

-0,6

0,6

1,2

1,8

2,4

Component2

resin-Pi

NaHCO3-Pi

NaOH-Pi

HCl-Pi

HClconc-Pi

BG

BG

BGBG

BG

BG

BG

BG

BG

BG

BG

BG

BG

BG

BG

IFA

IFA

IFA

IFA

IFA

IFA

IFA

IFA

IFA

IFA

IFA

IFA

IFA

-1,8 -1,5 -1,2 -0,9 -0,6 -0,3 0,3 0,6 0,9 1,2 1,5 1,8

Component 1

-3

-2,4

-1,8

-1,2

-0,6

0,6

1,2

1,8

2,4

Component2

FIGURE 2. Principal Component Analysis for soil P fractions data of the studied sites. IFA � ice-free area, BG � boundary of the glacier.

larger ratio the lower crystallinity (Beck and Elsenbeer, 1999), weregreatest in the IFA soil.

SOIL MINERALOGY COMPOSITION

Soil mineralogical composition was different between studiedsites. While in the BG site, XRD analysis showed the presence oflabradorite, quartz, and the P-bearing mineral hydroxyapatite, themajor mineral phases identified in the IFA were labradorite, quartz,and the secondary minerals hematite and chlorite-vermiculite-montmorillonite (Fig. 3; Table 5). Relative abundance of soil min-erals at the study sites, as judged from peak heights of the diffracto-grams, was as follows: BG: labradorite � quartz � hydroxyapatite;IFA: labradorite � hematite � quartz � chlorite-vermiculite-mont-morillonite (Fig. 3).

TABLE 3

Eigenvalues and cumulative percentage variance of soil phospho-rus fractions for the Principal Component Analysis carried out

with data of the studied sites.

Axes 1 2 3 4

Eigenvalues 2.0 1.2 0.9 0.6Total percentage variance 40.6 24.4 19.0 11.8Cumulative percentage variance 40.6 65.0 84.0 95.8


ALKALINE PHOSPHATASE AND FLUORESCEIN DIACETATEHYDROLYSIS. IMPLICATIONS IN THE GEOCHEMICALCYCLING OF P

There was a significant difference between sites with respectto enzyme activity and fluorescein diacetate hydrolysis (Table 6).The greatest values for both parameters were detected at the IFA.

TABLE 4

Values of iron and aluminum fractions (mmol kg1) in the bound-ary of the glacier (BG) and in the ice-free area (IFA).

Fraction BG IFA

FeP 3.01 � 0.39a 3.92 � 0.36a

FeO 53.31 � 1.95a 55.45 � 2.76a

FeDCB 107.77 � 3.67a 61.13 � 3.49b

FeT 164 � 4a 121 � 5b

AlP 3.39 � 1.50b 21.21 � 3.46a

AlO 5.45 � 2.39b 109.70 � 9.40a

AlDCB 20.21 � 0.62a 25.68 � 2.80a

AlT 29 � 3b 157 � 12a

FeO/FeDCB 0.50 � 0.02b 0.93 � 0.05a

AlO/AlDCB 0.30 � 0.14b 4.72 � 0.54a

Mean values � 1 SE followed by different letters in rows denotesignificant differences between sites. FeO-AlO, FeDCB-AlDCB, andFeP-Al-P � ammonium-oxalate, dithionite-citrate-bicarbonate, andpyrophosphate extractable Fe or Al, respectively; FeT-AlT � ∑FeO-AlO, FeDCB-AlDCB, and FeP-Al-P, respectively.


FIGURE 3. Typical X-ray diffraction patterns showing the three main peaks of the identified minerals at the studied sites. IFA � ice-free area, BG � boundary of the glacier, Lab � labradorite, Qz � quartz, Hem � hematite, HyAP � hydroxyapatite, Chl-Vrm-Mnt� chlorite-vermiculite-montmorillonite.

To investigate the relationships between geochemical and bio-logical cycling of P in each site, correlations between chemically de-fined P pools and the biological parameters (alkaline phosphataseactivity and fluorescein diacetate hydrolysis) were established. Atthe IFA, there was a positive correlation between the activity of APand the hydrolysis of FD (r � 0.95, P � 0.05; n � 15). For thissite, both biological parameters were positively correlated with the


organic and inorganic P fractions obtained in alkali extracts:NaHCO3 (r � 0.96 for AP and r � 0.91 for FD in inorganic pool;r � 0.90 for AP and r � 0.92 for FD in organic pool; P � 0.05,n � 15)and NaOH (r �0.98 for AP and r � 0.98 forFD in inorganicpool; r � 0.91 for AP and r � 0.81 for FD in organic pool;P � 0.05, n � 15). The relationships between microbial and enzy-matic activities and the soil P pools were not evident at the BG site.


TABLE 5

Chemical composition and d-spacing values (A) of the three main peaks of identified minerals by XRD analysis in each studied site.

Mineral/Identification card Chemical composition PM BG IFA

Labradorite/710748 (Na0.5Ca0.5) (Al1.5Si2.5O8) 3.20 3.21 3.203.18 3.18 3.184.04 4.04 4.03

Quartz/791910 SiO2 3.34 3.34 3.344.25 4.25 4.271.81 1.83 1.83

Hydroxiapatite/011008 Ca10(OH)2(PO4)6 2.79 2.833.44 3.471.84 1.87

Hematite/790007 Fe2O3 2.69 2.992.51 2.521.69 1.60

Chlorite-vermiculite-montmorillonite/390381 Na0.5Al6(Si,Al)8O20(OH)10H2O 3.50 3.477.70 7.954.44 4.66

PM � pure minerals, BG � boundary of the glacier, IFA � ice-free area.

DiscussionCHANGES IN P POOLS, Fe AND Al FRACTIONS, AND SOILMINERALOGY FROM THE BOUNDARY OF THE GLACIER TOICE-FREE AREA

It has been widely accepted that in the Antarctic region theextremely low temperatures and the limited availability of liquidwater restricts chemical weathering and consequently soil develop-ment (i.e. Ugolini, 1963; Chen and Blume, 1999; Gooseff et al.,2003; Bolter, 2011). However, in some locations, during the sum-mer, soil microclimatic conditions allow the presence of liquidwater and favor chemical weathering. This is the case of the ice-free areas at the Fildes Peninsula, which are exposed to a deepthawing period that lasts between 5 and 6 months each year (Chenand Blume, 1999). During this period, soils of these areas are sub-jected to greater temperatures and availability of free water thanat other sites in Antarctica (Zhao and Li, 1996; Chen and Blume,1999, 2000; Gooseff et al., 2003). In contrast, in terrestrial areasadjacent to subsurface ice, the liquid water content is limited due

TABLE 6

Alkaline phosphatase (AP) activity and the fluorescein diacetate(FD) hydrolysis of soils in the boundary of the glacier (BG) and

in the ice-free area (IFA).

Soilproperties Units BG IFA

AP �g p-NP g�1 2.92 � 0.95b 13.67 � 3.18a

dry soil h�1

FD �g fluorescein g�1 18.09 � 2.06b 49.67 � 16.87a

dry soil h�1

Mean values � 1 SE followed by different letters in rows denotesignificant differences between sites.


to the low air temperature and precipitation (Barrett et al., 2006).During summer, melting water from the glaciated areas may remainin a liquid state only during the warmest hours of the day andrefreezes as solar radiation decreases (Motta and Motta, 2004).Taking into account the differences in the microclimatic soil condi-tions of these two environments, and considering the implicationsof the water availability in soil chemical processes, we predictedin our first hypothesis that from the boundary of the glacier (BG)to the ice-free area (IFA) P associated with primary minerals shoulddecrease, while P bounded to secondary minerals should increase.To test this, we interpreted our results of soil P fractions alongwith the contents of secondary minerals (oxyhydroxides of Fe andAl) and soil mineralogy following the theory of Walker and Syers(1976). This theory proposes a conceptual model where availabilityand forms of soil P vary during its development as a consequenceof changes in mineral composition. According to the model, as soilevolution takes place, the weathering of primary minerals (Ca-bound phosphates) releases P, which is readily chemisorbed intothe secondary minerals (clay minerals as well as Fe and Al oxyhy-droxides).

Our results advance four lines of evidence that help us supportour first hypothesis. First, from BG to IFA, the concentration ofprimary mineral P (diluted HCl-Pi) declined, while the inorganicP chemisorbed and occluded to Fe/Al oxyhydroxides (NaOH- andconcentrated HCl-) increased. This pattern led to an inverse rela-tionship between the diluted HCl-Pi and NaOH-Pi at the IFA, butnot at the BG site. Such findings were consistent with those ob-tained using PCA, which showed that inorganic P pools were dis-tinct between the edge of the glacier and the ice-free area. Second,the greatest levels of Fe/Al oxyhydroxides were found in the IFAwhere the content of NaOH-Pi was also the greatest. Third, at theBG site, the content of AlT was sixfold lower than that of the FeT,and fivefold lower than the content of AlT in the soils of the IFA.


In the latter site, the contents of FeT and AlT were similar. Theobserved trend could be considered a signal of advanced soil devel-opment at the IFA because, in the soil environment, high contentsof secondary Al minerals are indicative of increased weathering(Hsu, 1977). Fourth, the presence of epigenetic minerals such ashematite and the intergrade chlorite-vermiculite-montmorillonitein the soil of the IFA is strong evidence that chemical alterationof bedrocks seems to be favored in this site. This was not the caseat the BG site, where soil mineralogy was characterized by thepresence of hydroxyapatite and the absence of chemical weatheringproducts. The soil mineralogy observed at the IFA was in goodagreement with the results obtained for other sites in the AntarcticPeninsula (Boyer, 1975; Kuzmann et al., 1998), where chemicalweathering is an important pedogenetic process.

Besides the above-mentioned, it is important to note that, ac-cording to the theory of Walker and Syers (1976), the chemicalalteration of primary minerals provides available P to the soil solu-tion. In this study, this was observed in the IFA soils, since a directrelationship between resin-Pi and the diluted HCl-Pi fraction wasobtained. Despite the fact that the alteration of primary mineralsincreased the available P at the IFA soils, such increase was notreflected in the organic P pool, which was very low and similarbetween the sites. This result is expected in an environment wherethe primary productivity is negligible and where, consequently, thecontent of soil organic matter is low (i.e. Hopkins et al., 2006a,2006b).

The observed differences in P cycling patterns as well as theformation of epigenetic minerals seem to confirm our first hypothe-sis. At this point it is important to mention that pedogenetic timewas not considered in our discussion, because differences in soilproperties could be explained as a function of time when soils arebeing formed under the same climatic condition (Kelly and Yonker,2005). However, this is not the case at the studied sites, since, aswas mentioned earlier, soils of the ice-free areas are exposed to aless extreme microclimatic soil condition than the terrestrial areasadjacent to subsurface ice.

Despite that soils of the IFA are significantly more developedthan soils of the BG site, in this study it is also important to recog-nize that the alteration of primary minerals in the IFA is still at anearly stage since the content of Ca-bound P (281.75 � 16.72 mgkg�1) is at the lower limit of the values reported by other authors(Blecker et al., 2006 [�267–349 mg kg�1]; Bate et al., 2008[�250–980 mg kg�1]) for soils of the Antarctic continent, wherethe weathering is more restricted.

Fe AND Al FRACTIONS AND THEIR IMPLICATIONS ON THESOIL P CYCLING

The non-crystalline forms of Fe and Al were found to be moreabundant in the IFA site, where the chemical weathering was moreintense (∑FeO-AlO: BG � 58.76 mmol kg�1, IFA � 165.15 mmolkg�1). As a result, this led to an increase of the non-crystallinityratios (AlO/AlDCB, FeO/FeDCB) in the IFA soils. Non-crystallineforms of Fe and Al (FeO-AlO) are considered the main sorbents ofphosphate, in relation to crystalline forms, due to their compara-tively larger specific surface area (Parfitt, 1989; Ugolini and Dahl-gren, 2002).


Whilst the soils of the IFA were enriched with non-crystallineminerals, crystalline forms of Fe were dominant at the BG site.This result seems to be closely related to chemical weathering.According to Ugolini and Dahlgren (2002), when volcanic materi-als, such as those that make up the Fildes Peninsula Group, areexposed to chemical weathering, the precipitation of non-crystal-line minerals is kinetically favored over precipitation of crystallineminerals. In comparison, crystalline minerals are formed at theexpense of metastable compounds (Ugolini and Dahlgren, 2002).These authors consider the time of exposure of the weatheringprocesses that are associated with warm and dry soil conditions asthe main factor promoting the formation of crystalline minerals.Soils of the BG site are not exposed to warm temperatures, but theyare subjected to longer periods of liquid water limitation, whichprobably favors the formation of crystalline minerals rather thannon-crystalline ones.

In addition to poorly crystalline minerals, the organicallybound forms of Fe and Al (FeP, AlP) are also active surfaces thatcontrol soil P retention capacity (Gerke and Hermann, 1992; Cha-con and Dezzeo, 2004; Chacon et al., 2005a, 2008). In this study,the content of these compounds was low as a result of the generallylow content of soil organic matter. However, AlP was more abun-dant in the soil from the IFA site than that from the BG site. Thisfinding, along with the great content of non-crystalline mineralsobtained for this site, allowed us to conclude that, potentially, IFAsoils have a greater P retention capacity than soils at the BG. Theimplications of these mineral surfaces on P dynamics have beenwell recognized for highly weathered acid soils (i.e. Schwertmannand Taylor, 1977; Parfitt, 1978; Chacon and Dezzeo, 2004; Chaconet al., 2005a, 2008). However, it is important to bear in mind thatthese mineral surfaces are positively charged over the whole pHrange commonly encountered in the soil (Hinsinger, 2001) and alsocontrol the P dynamics of alkaline soils (Matar et al., 1992; Bertrandet al., 1999; Hinsinger, 2001). In fact, in alkaline soils of the Antarc-tic continent, the increases of Al and Fe phosphates in soils whereweathering is less restricted have been explained by the presence ofnon-crystalline and crystalline Fe and Al oxyhydroxides (Blecker etal., 2006).

ALKALINE PHOSPHATASE AND MICROBIAL ACTIVITY ANDTHEIR RELATIONSHIP WITH THE BIOGEOCHEMICALCYCLING OF P

On the basis that biological activities in the terrestrial ecosys-tems of Antarctic region are largely controlled by abiotic factors(soil temperature and availability of liquid water), we formulatedour second hypothesis wherein we predicted an increase in micro-bial and enzymatic activities for the ice-free area. Indeed, AP activ-ity followed this expected trend. However, before we concludethat such behavior is promoted by the less extreme microclimaticconditions in the IFA, we ascertained within the context of ourresults, other concepts that could explain the observed pattern withthis enzyme.

On a global scale, it has been indicated that extracellular phos-phatase activities increase with soil organic matter concentration(Sinsabaugh et al., 2008). In this study, the content of soil organiccarbon at the IFA was 13-fold lower than the recorded value at theBG site (Benzo et al., unpublished data; samples collected in 2009),


even though the AP activity was fivefold greater at the IFA thanat the BG site. Comparing our findings with results obtained bySinsabaugh et al. (2008), it can be concluded that in our study sitesthere is no indication that soil organic carbon plays an importantrole in the activity of AP. However, other factors inherent to soilmatrix could be masking our results. Several studies have foundthat the interaction of phosphatase enzymes with non-crystallineAl and Fe oxides and clay minerals decreases enzyme activity whencompared to the non-immobilized enzyme activity (Huang et al.,1995; Rao et al., 1996, 2000; Shindo et al., 2002; Chacon et al.,2005b). As was already discussed above, soils of the IFA wereenriched with non-crystalline compounds, whereas crystallineforms dominated the soils of the BG site. Hence, from this mineral-ogical composition we could not explain the observed pattern ofthis soil enzyme. Generally speaking, most secondary minerals arefound in the fine fraction of the soil. According to Benzo et al.(unpublished data; samples collected in 2009), soil from the BGsite showed a relatively greater content of fine particles (clay) thanthat from the IFA. In both sites, the correlation of these data withthe values of AP activity obtained in this study was not significant(BG: r � �0.217, P� 0.05, n � 15; IFA: r � 0.117, P � 0.05,n � 15). This trend and the previous findings allow us to concludethat soil matrix is not driving the AP activity in the studied sites.

Once the influence of soil matrix on AP activity was discarded,it could be assumed that the activity was likely enhanced by soilmicroclimate conditions such as humidity and temperature. ForAntarctic soils this assumption is reasonable considering that in thisharsh environment microbial activities, like carbon and nitrogenmineralization and enzyme production (i.e. alkaline phosphatase),are favored in those areas where temperature allows greater soilwater availability (Barrett et al., 2005; Zeglin et al., 2009).

Considering the findings mentioned above and the fact thatFD hydrolysis has been widely used to determine the overall soilmicrobial activity potential (Nannipieri et al., 2003), it was notsurprising that this parameter followed the same behavior detectedfor AP activity. Unfortunately, to the best of our knowledge, forAntarctic soils there are no studies evaluating the influence of soilmicroclimate conditions on FD hydrolysis. However, for temperateecosystems it has been reported that suitable conditions of soiltemperature and moisture increased the levels of this biochemicalparameter (Sidari et al., 2008; Lillo et al., 2011; Reyes et al., 2011).

Finally, it is also important to analyze the positive relationshipbetween biological parameters (AP activity and FD hydrolysis) andboth organic and inorganic P pools obtained in alkaline extractantsof soils of the IFA. This striking finding suggests that in IFA soilsthe presence of liquid water allowed the co-occurrence of advancedchemical weathering and a greater biological activity. The conjunc-tion of both factors seems to have a strong influence over theP pools at the IFA.

ConclusionsThe changes in the inorganic P pools coupled with the increase

in secondary minerals at the IFA soils allowed us to conclude thatsoils from the IFA showed a greater chemical weathering intensitythan soils from the BG. This finding was consistent with the pedo-genic theory developed by Walker and Syers (1976). However, theprediction, which states that as soil evolution proceeds organic


P pools increase, could not be verified in this study due to thelack of variation between sites in this P pool. This discrepancy isexpected in the harsh environments of Antarctica where reducedinput of liquid water is responsible for negligible primary produc-tivity. The biochemical transformation of soil P was also favoredin the ice-free area. It is likely that the less restrictive microclimaticconditions, to which the soils of the ice-free areas are exposedduring the summer, have a considerable effect on the biogeochemi-cal cycling of soil phosphorus. Taken together, our findings demon-strated that, between the boundary of the glacier and the ice-freearea, there are differences in the patterns of soil P cycling. In ascenario of climate warming over the Antarctic Peninsula, this in-formation may contribute to the understanding of how the retreatof the glaciers and consequently the advance of the ice-free areascould be altering the biogeochemical cycling of essential nutrientsin this region.

AcknowledgmentsThis research was supported by the Venezuelan Antarctic Pro-

gram of the Ministerio del Poder Popular para Ciencia, Tecnologıae Innovacion (MCTI). Chacon thanks Maximiliano Bezada andDaniel Palacios, who helped in the fieldwork. We thank CristinaLull for her critical comments on an early version of this manu-script. We are very grateful to three anonymous reviewers for theircareful revision and valuable and critical commentaries about theoriginal version of the manuscript. We also wish to acknowledgeWerner Wilbert and Alessia Bastianoni for revising the Englishversion of the manuscript.

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MS accepted January 2013


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